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Comprehensive genome analysis of a novel actinobacterium with high potential for biotechnological applications, Nonomuraea aridisoli sp. nov., isolated from desert soil

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Abstract

During a study to isolate such actinobacteria with unique metabolic potential, a novel actinobacterium, designated KC333T, was isolated from a soil sample collected from the Karakum Desert, Turkmenistan. The taxonomic position of the strain was investigated using a polyphasic approach. Phylogenetic analysis of the 16S rRNA gene sequence showed that the strain was most closely related to Nonomuraea terrae CH32T (99.0% sequence similarity), Nonomuraea maritima FXJ7.203 T (98.9%), Nonomuraea candida HMC10T (98.7%) and Nonomuraea gerenzanensis ATCC 39727 T (98.6%), and is therefore considered to represent a member of the genus Nonomuraea. However, the average nucleotide identity and digital DNA-DNA hybridization based on whole-genome sequences between strain KC333T and close relatives demonstrated that it represents a novel species of the genus Nonomuraea. The major cellular fatty acids of strain KC333T were iso-C16: 0, C17:0 10-methyl and iso-C16: 0 2OH. Strain KC333T contained meso-diaminopimelic, mannose, madurose and ribose in the cell-wall peptidoglycan. The predominant menaquinones were MK-9(H4) and MK-9(H6). The genome size of strain KC333T is approximately 9.86 Mb, and the genomic DNA G + C content of the strain is 71.3%. In addition to the polyphasic characterisation, comprehensive genome analysis for gene clusters encoding carbohydrate-active enzymes and bioactive secondary metabolites as well as CRISPR-associated sequences revealed the high biotechnological potential of the strain. Based on evidence collected from the genotypic, phenotypic, and phylogenetic analyses, a novel species, Nonomuraea aridisoli sp. nov. is proposed with KC333T (= DSM 107062 T = JCM 32584 T = KCTC 49111 T) as the type strain.

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Data availability

The GenBank accession number for the 16S rRNA gene sequence of strain KC333T is MG770648. The GenBank accession number for the draft genome sequence of strain KC333T is POUD00000000.

Abbreviations

CAZymes:

Carbohydrate active enzymes

ISP 2:

International Streptomyces project

NPRS:

Nonribosomal peptide synthetases

PKS:

Polyketide synthase

TYGS:

Type strain genome server

References

  • Alanjary M et al (2017) The antibiotic resistant target seeker (ARTS), an exploration engine for antibiotic cluster prioritisation and novel drug target discovery. Nucleic Acids Res 45:W42–W48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ay H (2020) Nonomuraea terrae sp. nov., isolated from arid soil. Arch Microbiol 202:2197–2205

    Article  CAS  PubMed  Google Scholar 

  • Ay H, Saygin H, Sahin N (2020) Phylogenomic revision of the family Streptosporangiaceae, reclassification of Desertactinospora gelatinilytica as Spongiactinospora gelatinilytica comb. nov. and a taxonomic home for the genus Sinosporangium in the family Streptosporangiaceae. Int J Syst Evol Microbiol 70:2562–2572

    Article  Google Scholar 

  • Aziz RK et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75

    Article  PubMed  PubMed Central  Google Scholar 

  • Bankevich A et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belknap KC, Park CJ, Barth BM, Andam CP (2020) Genome mining of biosynthetic and chemotherapeutic gene clusters in Streptomyces bacteria. Sci Rep 10:2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blin K et al (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238

    Article  CAS  PubMed  Google Scholar 

  • Cao P et al (2019) Nonomuraea lactucae sp. nov., a novel actinomycete isolated from rhizosphere soil of lettuce (Lactuca sativa). Int J Syst Evol Microbiol 69:316–321

    Article  CAS  PubMed  Google Scholar 

  • Chiba S, Suzuki M, Ando K (1999) Taxonomic re-evaluation of ‘Nocardiopsis’ sp K-252T (= NRRL 15532T): a proposal to transfer this strain to the genus Nonomuraea as Nonomuraea longicatena sp. nov. Int J Syst Evol Microbiol 49:1623–1630

    Article  Google Scholar 

  • Collins MD (1985) 11 analysis of isoprenoid quinones. In: Bergan T (ed) Methods in microbiology, vol 18. Elsevier, Amsterdam, pp 329–366

    Google Scholar 

  • Cundliffe E, Demain AL (2010) Avoidance of suicide in antibiotic-producing microbes. J Ind Microbiol Biotechnol 37:643–672

    Article  CAS  PubMed  Google Scholar 

  • D’Argenio V et al (2016) The complete 12 Mb genome and transcriptome of Nonomuraea gerenzanensis with new insights into its duplicated “magic” RNA polymerase. Sci Rep 6:1–13

    Article  Google Scholar 

  • Darzi Y, Letunic I, Bork P, Yamada T (2018) iPath3. 0: interactive pathways explorer v3. Nucleic Acids Res 46:W510–W513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis JJ et al (2016) PATtyFams: protein families for the microbial genomes in the PATRIC database. Front Microbiol 7:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong H, Yue X, Yan B, Gao W, Wang S, Li Y (2020) Improved A40926 production from Nonomuraea gerenzanensis using the promoter engineering and the co-expression of crucial genes. J Biotechnol 324:28–33

    Article  CAS  PubMed  Google Scholar 

  • Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668

    Article  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Feng Y-Z et al (2019) Bailinhaonella thermotolerans gen. nov., sp. nov., a new member of the order Streptosporangiales. Int J Syst Evol Microbiol 69:1903–1909

    Article  CAS  PubMed  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • Goldstein BP et al (1987) A40926, a new glycopeptide antibiotic with anti-Neisseria activity. Antimicrob Agents Chemother 31:1961–1966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodfellow M (1971) Numerical taxonomy of some nocardioform bacteria. Microbiology 69:33–80

    CAS  Google Scholar 

  • Gordon RE, Barnett DA, Handerhan JE, Pang CH-N (1974) Nocardia coeliaca, Nocardia autotrophica, and the nocardin strain. Int J Syst Evol Microbiol 24:54–63

    Google Scholar 

  • Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA–DNA hybridisation values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91

    Article  CAS  PubMed  Google Scholar 

  • Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57

    Article  PubMed  PubMed Central  Google Scholar 

  • Igarashi M et al. (2021) Sealutomicins, new enediyne antibiotics from the deep-sea actinomycete Nonomuraea sp. MM565M-173N2. J Antibiot. https://doi.org/10.1038/s41429-020-00402-1

  • Jones KL (1949) Fresh isolates of actinomycetes in which the presence of sporogenous aerial mycelia is a fluctuating characteristic. J Bacteriol 57:141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jorgensen JH, Turnidge JD, Washington JA (1999) Antibacterial susceptibility tests: dilution and disk diffusion methods. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH (eds) Manual of clinical microbiology. American Society for Microbiology, Washington DC, pp 1526–1543

    Google Scholar 

  • Jukes T, Cantor C (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Chapter  Google Scholar 

  • Kämpfer P (2012) Genus VI. Nonomuraea. In: Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki K, Ludwig W, and Whitman WB (eds) Bergey's Manual of Systematic Bacteriology. pp. 1844–1861

  • Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005

    Article  Google Scholar 

  • Katoh K, Standley D (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol and Evol 30:772–780

    Article  CAS  Google Scholar 

  • Kroppenstedt RM (1982) Separation of bacterial menaquinones by HPLC using reverse phase (RP18) and a silver loaded ion exchanger as stationary phases. J Liq Chromatogr 5:2359–2367

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Küster E, Williams S (1964) Selection of media for isolation of streptomycetes. Nature 202:928–929

    Article  Google Scholar 

  • Lane D (1991) 16S/23S rRNA sequencing . In: Stackebrandt E, Goodfellow M. (eds) Nucleic acid techniques in bacterial systematics New York, USA: Wiley; 1991; pp.115–175

  • Lechevalier MP, Lechevalier H (1970) Chemical composition as a criterion in the classification of aerobic actinomycetes. Int J Syst Evol Microbiol 20:435–443

    CAS  Google Scholar 

  • Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Gui Y-h, Xu Q-h, Lin H-w, Lu Y-h (2019) Spongiactinospora rosea gen. nov., sp. nov., a new member of the family Streptosporangiaceae. Int J Syst Evol Microbiol 69:427–433

    Article  CAS  PubMed  Google Scholar 

  • Lipun K, Teo WFA, Suksaard P, Pathom-Aree W, Duangmal K (2020) Nonomuraea antri sp. nov., an actinomycete isolated from cave soil in Thailand. Int J Syst Evol Microbiol 70:5296–5303

    Article  CAS  PubMed  Google Scholar 

  • Liu K-a, Gai Y, Fayyaz A, Zhang G, Liu M, Wang Z (2020) Genomic and morphological characteristics of the cold-adapted bacteria Mycetocola saprophilus provide insights into the pathogenesis of soft rot in Flammulina velutipes. Biotechnol Biotechnol Equip 34:885–897

    Article  CAS  Google Scholar 

  • Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:2182

    Article  PubMed  PubMed Central  Google Scholar 

  • Minnikin D, O’donnell A, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett J, (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241

    Article  CAS  Google Scholar 

  • Monciardini P, Sosio M (2004) Reclassification as a Nonomuraea sp. of the strain ATCC 39727, producing the glycopeptide antibiotic A40926. J Antibiot 57:68–70

    Article  CAS  Google Scholar 

  • Mungan MD, Alanjary M, Blin K, Weber T, Medema MH, Ziemert N (2020) ARTS 2.0: feature updates and expansion of the antibiotic resistant target seeker for comparative genome mining. Nucleic Acids Res 48:W546–W552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakaew N, Sungthong R, Yokota A, Lumyong S (2012) Nonomuraea monospora sp. nov., an actinomycete isolated from cave soil in Thailand, and emended description of the genus Nonomuraea. Int J Syst Evol Microbiol 62:3007–3012

    Article  CAS  PubMed  Google Scholar 

  • Nazari B, Forneris CC, Gibson MI, Moon K, Schramma KR, Seyedsayamdost MR (2017) Nonomuraea sp. ATCC 55076 harbours the largest actinomycete chromosome to date and the kistamicin biosynthetic gene cluster. Med Chem Commun 8:780–788

    Article  CAS  Google Scholar 

  • Nouioui I et al (2018) Genome-based taxonomic classification of the phylum Actinobacteria. Front Microbiol 9:2007

    Article  PubMed  PubMed Central  Google Scholar 

  • Ou Y et al (2020) Nonomuraea nitratireducens sp. nov., a new actinobacterium isolated from Suaeda australis Moq. rhizosphere. Int J Syst Evol Microbiol 70:5026–5031

    Article  CAS  PubMed  Google Scholar 

  • Primahana G, Risdian C, Mozef T, Sudarman E, Köck M, Wink J, Stadler M (2020) Nonocarbolines A–E, β-carboline antibiotics produced by the rare actinobacterium Nonomuraea sp. from Indonesia. Antibiotics 9:126

  • Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol

  • Saricaoglu S et al (2020) Nonomuraea basaltis sp. nov., a siderophore-producing actinobacteria isolated from surface soil of basaltic parent material. Arch Microbiol 202:1535–1543

    Article  CAS  PubMed  Google Scholar 

  • Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI technical note 101. Newark, DE: MIDI inc

  • Saygin H, Ay H, Guven K, Cetin D, Sahin N (2019) Desertiactinospora gelatinilytica gen. nov., sp. nov., a new member of the family Streptosporangiaceae isolated from the Karakum Desert. Antonie Van Leeuwenhoek 112:409–423

    Article  CAS  PubMed  Google Scholar 

  • Saygin H et al (2020) Polyphasic classification of Nonomuraea strains isolated from the Karakum Desert and description of Nonomuraea deserti sp. nov., Nonomuraea diastatica sp. nov., Nonomuraea longispora sp. nov. and Nonomuraea mesophila sp. nov. Int J Syst Evol Microbiol 70:636–647

    Article  CAS  PubMed  Google Scholar 

  • Shirling ET, Gottlieb D (1966) Methods for characterisation of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Skinnider MA, Merwin NJ, Johnston CW, Magarvey NA (2017) PRISM 3: expanded prediction of natural product chemical structures from microbial genomes. Nucleic Acids Res 45:W49–W54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Staneck JL, Roberts GD (1974) Simplified approach to identification of aerobic actinomycetes by thin-layer chromatography. Appl Environ Microbiol 28:226–231

    Article  CAS  Google Scholar 

  • Sungthong R, Nakaew N (2015) The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. J Basic Microbiol 55:554–565

    Article  PubMed  Google Scholar 

  • van Bergeijk DA, Terlouw BR, Medema MH, van Wezel GP (2020) Ecology and genomics of Actinobacteria: new concepts for natural product discovery. Nat Rev Microbiol1–13

  • Waksman SA (1961) The Actinomycetes. vol. II. Classification, identification and descriptions of genera and species. Baltimore: Williams & Wilkins

  • Waksman SA (1967) The Actinomycetes. A summary of current knowledge. Ronald Press, New York

    Google Scholar 

  • Wattam AR et al (2017) Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 45:D535–D542

    Article  CAS  PubMed  Google Scholar 

  • Wayne L et al (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 37:463–464

    Article  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams S, Goodfellow M, Alderson G, Wellington E, Sneath P, Sackin M (1983) Numerical classification of Streptomyces and related genera. Microbiology 129:1743–1813

    Article  CAS  Google Scholar 

  • Yang T et al (2019) Akazamicin, a cytotoxic aromatic polyketide from marine-derived Nonomuraea sp. J Antibiot 72:202–209

    Article  CAS  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017a) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon S-H, Ha S-m, Lim J, Kwon S, Chun J (2017b) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286

    Article  CAS  PubMed  Google Scholar 

  • Yushchuk O, Andreo-Vidal A, Marcone GL, Bibb M, Marinelli F, Binda E (2020) New molecular tools for regulation and improvement of A40926 glycopeptide antibiotic production in Nonomuraea gerenzanensis ATCC 39727. Front Microbiol 11:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang H et al (2018) dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:W95–W101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Wang Y, Ruan J (1998) Reclassification of Thermomonospora and Microtetraspora. Int J Syst Evol Microbiol 48:411–422

    Google Scholar 

  • ZoBell CE (1941) Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J Mar Res 4:41–75

    Google Scholar 

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Acknowledgements

Genome sequencing was provided by MicrobesNG (http://www.microbesng.uk).

Funding

This research was supported by Ondokuz Mayis University (OMU), Project No. PYO.FEN.1901.16.001.

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Authors and Affiliations

  1. Department of Molecular Biology and Genetics, Faculty of Sciences and Arts, Ondokuz Mayis University, 55139, Samsun, Turkey

    Hayrettin Saygin, Hilal Ay & Nevzat Sahin

  2. Department of Biology, Faculty of Science and Arts, Ondokuz Mayis University, 55139, Samsun, Turkey

    Hayrettin Saygin

  3. Department of Biology, Faculty of Science, Eskisehir Technical University, 26555, Eskisehir, Turkey

    Kiymet Guven

  4. Division of Science Education, Department of Mathematics and Science Education, Gazi University, 06500, Ankara, Turkey

    Demet Cetin

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Contributions

HS and NS designed the study. HS and HA carried out physiological experiments. HS, HA, and KG designed chemotaxonomic analyses. HS and HA carried out genome sequence analysis. DC carried out scanning electron microscopy analysis. NS wrote the paper.

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Correspondence to Nevzat Sahin.

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Saygin, H., Ay, H., Guven, K. et al. Comprehensive genome analysis of a novel actinobacterium with high potential for biotechnological applications, Nonomuraea aridisoli sp. nov., isolated from desert soil. Antonie van Leeuwenhoek 114, 1963–1975 (2021). https://doi.org/10.1007/s10482-021-01654-z

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